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Effects of external lithium on the physiology of Limulus ventral photoreceptors

Published online by Cambridge University Press:  02 June 2009

Peter M. O'Day
Affiliation:
Institute of Neuroscience, University of Oregon, Eugene
Cynthia L. Phillips
Affiliation:
Iinstitute of Molecular Biology, University of Oregon, Eugene

Abstract

We have examined some of the physiological effects associated with the replacement of extracellular Na+ with Li+ in nominally Ca2+-free saline in the ventral photoreceptors of the horseshoe crab Limulus polyphemus. We observed that replacement of Na+ saline with Li+ saline induced larger voltage-activated inward currents with similar voltage dependence. These currents were absent in Tris+ saline. Anode-break excitation was maintained in Li+ saline but blocked in Tris+ saline. Regenerative events associated with quantum bumps in dark-adapted cells illuminated with dim lights were maintained in Li+ saline. Regenerative events associated with responses to moderately bright illumination were also maintained in Li+ saline. The post-illumination hyperpolarization associated with the Na+/K+-exchange pump (Brown & Lisman, 1972) was present after brief exposure to Li+ saline but disappeared after longer exposure. Following return to Na+ saline, the post-illumination hyperpolarization reappeared. We conclude that (1) Li+ permeates the voltage-dependent Na+ channel, GNa(V), in the photoreceptor plasma membrane; (2) Li+ supports voltage-activated physiological events normally mediated by Na+; and (3) Li+ substitution briefly supports and later inhibits the electrogenic effects of the Na+/K+-exchange pump. The effects of external Li+ on cellular physiology have implications for the interpretation of other studies employing Li+ extracellularly.

Type
Research Articles
Copyright
Copyright © Cambridge University Press 1991

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References

Adams, D.J., Smith, S.J. & Thompson, S.H. (1980). Ionic currents in molluscan neurons. Annual Reviews of Neuroscience 3, 141167.CrossRefGoogle Scholar
Adolph, A. (1964). Spontancous slow potential fluctuations in the Limulus photoreceptor. Journal of General Physiology 48, 297322.CrossRefGoogle Scholar
Baylor, D.A. & Nicholls, J.G. (1969). Changes in extracellular potassium concentration produced by neuronal activity in the central nervous system of the leech. Journal of Physiology 203, 555569.CrossRefGoogle ScholarPubMed
Berridge, M.J., Downes, C.P. & Hanley, M.R. (1982). Lithium amplifies agonist dependent phosphatidylinositol responses in brain and salivary glands. Biochemical Journal 206, 587595.CrossRefGoogle ScholarPubMed
Berridge, M.J., Downes, C.P. & Hanley, M.R. (1989). Neural and developmental actions of lithium: a unifying hypothesis. Cell 59, 411419.CrossRefGoogle Scholar
Berridge, M.J. & Irvine, R.F. (1984). Inositol trisphosphate, a novel second messenger in cellular signal transduction. Nature 312, 315321.CrossRefGoogle ScholarPubMed
Blaustein, M.P. & Hodgkin, A.L. (1969). The effect of cyanide on the efflux of calcium from squid axons. Journal of Physiology 200, 497527.CrossRefGoogle ScholarPubMed
Brown, J.E. & Lisman, J.E. (1972). An electrogenic sodium pump in Limulus ventral photoreceptor cells. Journal of General Physiology 59, 720740.CrossRefGoogle ScholarPubMed
Brown, J.E. & Mote, M.I. (1974). Ionic dependence of reversal voltage of the light response in Limulus ventral photoreceptors. Journal of General Physiology 63, 337350.CrossRefGoogle ScholarPubMed
Brown, J.E., Rubin, L.J., Ghalayini, A.J., Tarver, A.L., Irvine, R.F., Berridge, M.J. & Anderson, R.E. (1984). Myo-inositol polyphosphate may be a messenger for visual excitation in Limulus ventral photoreceptors. Nature 311, 160162.CrossRefGoogle Scholar
Calman, B.G. & Chamberlain, S.C. (1982). Distinct lobes of Limulus ventral photoreceptors, II. Structure and ultrastructure. Journal of General Physiology 80, 839862.CrossRefGoogle ScholarPubMed
Chinn, K. & Lisman, J.E. (1984). Light reduces the voltage-dependent inward current in Limulus ventral photoreceptors. Journal of General Physiology 84, 463473.CrossRefGoogle ScholarPubMed
Clark, A.W., Millecchia, R. & Mauro, A. (1969). The ventral photoreceptor cells of Limulus, I: The microanatomy. Journal of General Physiology 54, 289309.CrossRefGoogle ScholarPubMed
Coles, J.A. & Tsacopolous, M. (1979). Potassium activity in photoreceptors, glial cells and extracellular space in the drone retina: changes during photostimulation. Journal of Physiology 290, 525549.CrossRefGoogle ScholarPubMed
Devary, O., Heichal, O., Blumenfeld, A., Cassel, D., Suss, E., Barash, S., Rubinstein, C.T., Minke, B. & Selinger, Z. (1987). Coupling of photoexcited rhodopsin to inositol phospholipid hydrolysis in fly photoreceptors. Proceedings of the National Academy of Sciences of the U.S.A. 84, 69396943.CrossRefGoogle ScholarPubMed
Dodge, F.A., Knight, B.W. & Toyoda, J. (1968). Voltage noise in Limulus visual cells. Science 160, 8890.CrossRefGoogle ScholarPubMed
Edwards, C. (1982). The selectivity of ion channels in nerve and muscle. Neuroscience 7, 13351366.CrossRefGoogle ScholarPubMed
Fein, A. & Charlton, J.S. (1978). Recovery from adapting light in Limulus ventral photoreceptors. Brain Research 153, 585590.CrossRefGoogle ScholarPubMed
Fein, A., Payne, R., Corson, D.W., Berridge, M.J. & Irvine, R.F. (1984). Photoreceptor excitation and adaptation by inositol 1,4,5-trisphosphate. Nature 311, 157160.CrossRefGoogle ScholarPubMed
Fein, A. & Tsacopoulos, M. (1988). Light-induced oxygen consumption in Limulus ventral photoreceptors does not result from a rise in the intracellular sodium concentration. Journal of General Physiology 91, 515527.CrossRefGoogle Scholar
Holt, C.E. & Brown, J.E. (1972). Ion fluxes in photoreception in Limulus polyphemus ventral eye, I. The response of potassium efflux to light. Biochimica et Biophysica Acta 274, 140157.CrossRefGoogle ScholarPubMed
Johnson, E.C. & O'Day, P.M. (1991). Effects of lithium ion on light-induced excitation of Limulus ventral photoreceptors (Manuscript in preparation).Google Scholar
Keynes, R.D. & Swan, R.C. (1959). The effect of external sodium on sodium fluxes in frog skeletal muscle. Journal of Physiology 147, 591625.CrossRefGoogle ScholarPubMed
Koike, H., Brown, H.M. & Hagiwara, S. (1971). Hyperpolarization of a barnacle photoreceptor membrane following illumination. Journal of General Physiology 57, 723737.CrossRefGoogle ScholarPubMed
Lisman, J.E. & Brown, J.E. (1972). The effects of intracellular iontophoretic injection of calcium and sodium ions on the light response of Limulus ventral photoreceptors. Journal of General Physiology 59, 701719.CrossRefGoogle ScholarPubMed
Lisman, J.E., Fain, G.L. & O'Day, P.M. (1982). Voltage-dependent conductances in Limulus ventral photoreceptors. Journal of General Physiology 79, 187209.CrossRefGoogle ScholarPubMed
Millecchia, R. & Mauro, A. (1969). The ventral photoreceptor cells of Limulus II. The basic photoresponse. Journal of General Physiology 54, 310330.CrossRefGoogle ScholarPubMed
Mullins, L.J. (1977). A mechanism of Na+/Ca2+-exchange. Journal of General Physiology 70, 681696.CrossRefGoogle Scholar
O'Day, P.M. & Gray-Keller, M.P. (1989). Evidence for electrogenic Na+/Ca2+-exchange in Limulus ventral photoreceptors. Journal of General Physiology 93, 473492.CrossRefGoogle ScholarPubMed
O'Day, P.M., Gray-Keller, M.P. & Lonergan, M. (1991a). Physiological roles of Na+/Ca2+ exchange in Limulus ventral photoreceptors. Journal of General Physiology 97, 369391.CrossRefGoogle ScholarPubMed
O'Day, P.M., Johnson, E.C. & Baumgard, M. (1991b). Effects of lithium, calcium, and PDE-inhibitors on excitation of Limulus ventral photoreceptors. Biophysical Journal 59, 540a.Google Scholar
O'Day, P.M. & Keller, M.P. (1987). Effects of Li+-substitution and Li+-injection on light responses in Limulus ventral photoreceptors. Investigative Ophthalmology and Visual Science (Suppl.) 28, 402 (Abstracts).Google Scholar
O'Day, P.M., Lisman, J.E. & Goldring, M. (1982). Functional significance of voltage-dependent conductances in Limulus ventral photoreceptors. Journal of General Physiology 79, 211232.CrossRefGoogle ScholarPubMed
Pepose, J.S. & Lisman, J.E. (1978). Voltage-sensitive potassium channels in Limulus ventral photoreceptors. Journal of General Physiology 71, 101120.CrossRefGoogle ScholarPubMed
Skou, J.C. (1965). Enzymatic basis for active transport of Na+ and K+ across cell membrane. Physiological Reviews 45, 596617.CrossRefGoogle Scholar
Wong, F., Knight, B. & Dodge, F.A. (1982). Adapting bump model for ventral photoreceptors of Limulus. Journal of General Physiology 79, 10891113.CrossRefGoogle ScholarPubMed
Wong, F. (1978). Nature of light-induced conductance changes in ventral photoreceptors of Limulus. Nature 276, 7679.CrossRefGoogle ScholarPubMed